By Linda P. Case

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shelter dogs

Dogs are talented observers of human body language. Dog folks attest to this via boatloads of anecdotal stories and home videos that we are happy to share (and over-share) with others. But more importantly for the purposes of The Science Dog, it is the results of an additional boatload of controlled research studies that support our belief that dogs are paying attention to us.

Getting the Point: Human pointing gestures have emerged as a research litmus test for measuring the dog’s ability to understand human communication signals. To date, there are more than 50 published papers that report about this talent in dogs. Researchers have compared pointing comprehension between dogs and socialized and unsocialized wolves, between dogs living as pets and those living in shelters, among puppies and dogs of different ages, using various types of pointing (hand, eyes, body position) and when the pointing person is either familiar or unfamiliar to the dog. Though results vary and there are a number of nuanced points (literally) to be made, there is no longer any doubt.

Dogs are good at this pointing stuff. We point to something, they will look there.

Which of course, begs the question, how do dogs attain this very special talent in the first place? Are they born with it or is it primarily a learned phenomenon? Two general hypotheses have been put forward. The first emphasizes the importance of genetic preparedness and domestication while the second leans more heavily upon the influence of an individual dog’s life experiences:

Domestication Hypothesis: This explanation focuses on the genetic basis of social cognition and posits that the processes of domestication plus natural and artificial selection have resulted in a species that is genetically predisposed to attend to and comprehend human behavior and communication cues. Studies showing that dogs out-performed socialized wolves in cue-following tasks and unsolvable problem paradigms provide support for this theory.

Two-Stage Hypothesis: This hypothesis posits that a dog’s relationship with his or her human companions and opportunities to learn about human communication signals are essential for cue-following success. While followers of this theory agree that dogs have a genetic predisposition for bonding with humans, they maintain that the ability to understand and respond to our communication signals is gained primarily through living with and learning from human caretakers. Studies showing that some highly socialized wolves actually outperform some dogs in their ability to understand our signals support this view.

One of the biggest challenges in parsing the influences of domestication/selection and ontogeny/learning on the dog’s social cognition skills is finding truly representative samples (groups of dogs). For example, studies that have compared shelter dogs with dogs living in homes have been used to examine the influences of socialization and learning. The supposition is that shelter dogs are less socialized and have had few opportunities to learn from humans and so represent a group in which genetic influences would prevail. However, the background of shelter dogs is often unknown and a substantial number may have lived in homes and have had previous training. Similarly, a dog who lives in a home may receive widely varying degrees of human interaction and opportunities to learn social cues. These difficulties are probably responsible, at least in part, for the inconsistent results that studies comparing social cognition in shelter dogs and pet dogs have produced.

Representative samples: A newly published study by Biagio D’Aniello’s team at the University of Naples controlled for this particular problem by studying a group of dogs who were exclusively kennel-raised and who had experienced very limited opportunity to learn from human caretakers. (For more information about the importance of representative samples see “Your Face is Gonna Freeze Like That“).

The Study: Two groups of dogs were studied. The first included 11 Labrador and Golden Retrievers living at the FOOF kennel in Naples, Italy (kennel dogs). Although well cared for and socialized with other dogs, the dogs had very limited social interactions with people, no training and no daily opportunities to learn from humans. Each of these dogs was age-, sex- and breed-matched with a dog who had lived with a family in a home from puppyhood (pet dogs). During the pre-test period, all of the dogs learned to anticipate the presence of a food morsel in a small bowl. During the test phase, an experimenter pointed to one of two possible bowls while either kneeling close to the bowl (proximal test) or standing approximately 2 feet away from the bowls (distal test). The study used dynamic pointing, which means that the experimenter continued to hold the pointing gesture after the dog was released and allowed to make a choice of one of the two bowls. Trials were repeated 16 times with an additional 8 control trials. Dogs were scored as either correct (choosing the bowl that the experimenter was pointing to), incorrect (choosing the other bowl), or no-choice (not approaching either bowl).

Results: The pet dog group greatly outperformed the kennel dog group in their ability to understand both types of pointing gesture:

10 of 11 (91 %) of the pet dogs performed at greater than chance levels (i.e. chose correctly more than chance would predict) when the experimenter was in either position (kneeling and close or standing and further away).

In contrast, only 1 kennel dog (9 %) performed greater than chance when the experimenter was close to the bowls and none of the kennel dogs were successful when the pointer was standing further away.

A relatively high number of “no-choice” responses were observed, with these occurring at a much higher rate in kennel dogs than in pet dogs. When a separate analysis was conducted that removed “no choice” responses from the data, the success differences between the two groups of dogs were maintained, although a smaller number of trials were analyzed.

Comparisons between the two groups of dogs in overall success at understanding human pointing gestures showed that the pet dogs were significantly more successful at understanding both types of pointing (proximal and distal) than the kennel dogs.

Conclusions: These results support the hypothesis that human socialization and learning are necessary for dogs to comprehend human pointing gestures. Very low degrees of human socialization, even in dogs who are well-cared for and socialized to other dogs, results in dogs who do not understand or respond to pointing gestures. The authors conclude that while the influence of domestication on the dog’s ability to understand our communication cues is not insignificant, socialization and having opportunities to learn from human caretakers is essential.

Here’s why: Consider how frequently during a given day that you communicate with your dog via gestures and pointing signals that are not formally trained cues. These body language cues function in daily life to provide your dog with information (“Look Ally, you missed that piece of muffin on the floor“), communicate direction (“Chippy, we are going to the car, not out to the pool”) or about current plans (“Com’on Vinny, time to cuddle on the couch”). These cues are informal and often times completely unconscious on our part, but our dogs pay attention to them, understand what they mean and respond appropriately. These are our dogs – the dogs who “get the point”. We all co-develop a common language with our dogs that is made up of pointing gestures, body cues, facial expressions and key phrases. Take a moment to think about these and identify a few that you know that you use often in your home and that your dog readily responds to. There are bunches.

Now, consider dogs living in shelters: Some shelter dogs will definitely “get the point” if they had prior opportunities to bond with people and learn about the significance of human body language. Others, however, may lack this background and will miss the point. I would venture that the previous group are going to fare better in adoptive homes than the latter group. A shelter dog who has learned that human communication signals are worth paying attention to is likely to be perceived positively by his or her new owner because the dog will be aware of the significance of human body language, gestures and non-verbal communication cues. Subsequently, the new owner is likely to perceive such behaviors as a dog who is being sensitive to the family dynamics, is bonding well, and is trainable. End result – a good match and dog stays in home.

Conversely, the shelter dog who has not had an opportunity to learn about human communication cues will be at real disadvantage when he enters his new home. He will be less likely to attend to his new human’s gestures and body language cues simply because he has never learned that such gestures are worth paying attention to. While the new dog owner may not think of this in terms of his dog “attending” to his body language or communication cues per se, he will most likely notice that his dog is not paying much attention to him or responding to him. Subsequently, the new owner may perceive this as his new dog being too independent, not loving enough, aloof, or even untrainable. End result – the dog may not stay long.

If the direction that these data are pointing is correct and dogs need opportunities to learn about human communication skills (i.e. they are not purely a by-product of domestication), then it is quite possible that the benefits of shelter socialization and training programs go well beyond producing better mannered dogs who sit or lie down on command (not that there is anything wrong with those things, of course). I would expect that these less tangible benefits of shelter training and socialization programs, specifically dogs learning the significance of paying attention to human communication cues, may be more important for dogs in the long run than the more obvious benefits of teaching dogs manners and responses to cues.

So, to those of you who are working with shelter dogs to improve their lives and their chances of adoption, Keep on Keepin’ on – Science is behind you.

SHELTER DOG TRAINING – BENEFITS TO SOCIAL COGNITION SKILLS? (Photo courtesy of the Center for Shelter Dogs, Cummings School of Veterinary Medicine at Tufts University)

All four of our dogs like cats and are especially smitten with our current cat, Pete. They play with Pete, go for walks with him and sleep with him.

CHIPPY AND PETE ENJOY AN AFTERNOON NAP

Lucky for us, (and for Pete), our dogs would definitely fall within the category of ailurophile (cat lover).

COOPER CASE, CARD-CARRYING AILUROPHILE

But, of course, this is not true of all dogs. Many are not fans of the feline race.

Some dogs are afraid of cats.

Others hate cats.

And some are conflicted.

Where a particular dog falls on the cat-loving to cat-hating scale is an important consideration for shelter staff and rescue folks who are attempting to place dogs into suitable homes. In many cases, they have no way to know whether or not a particular dog is safe with cats. While there are several behavior assessment protocols available, none include a validated test that predicts how a dog behaves towards cats. Since this can vary dramatically and because aggressive or predatory behavior towards cats can have fatal consequences, this is important information to know. Recently, Dr. Christy Hoffman and the Canine Research Team at Canisius College in Buffalo, New York, studied cat-loving and cat-hating dogs to determine what behavioral cues might be helpful in developing a reliable test for ailurophilia (or its opposite) in dogs.

The Study: They hypothesized that dogs who had a history of having either harmed or killed cats or other small animals would be more attentive to visual, auditory and visual cat cues than would dogs who had no such history. They also speculated that, given the dog’s highly refined senses of smell and hearing, dogs would generally be highly sensitive to cat sounds and cat smells. They examined the reactions of 69 adult dogs of varying breeds and breed-mixes to a visual cue (animated white kitty toy), an auditory cue (recordings of cat meows and growls), and an olfactory/visual cue (a tube of cat urine placed inside the cat toy). Each of these experimental conditions was paired with a control (white pillow case containing a motorized ball, recording of coins falling, and urine tube placed inside pillow case, respectively). The study design involved exposing dogs to each stimulus and its paired control (for example, the animated cat toy and the animate pillow case) and recording responses.

Results: The dogs reacted differently to the various types of cat stimuli, and dogs who were not fond of cats behaved somewhat differently than those who liked (and lived with) cats:

Altogether, dogs were more sensitive to cat vocalizations than they were to the sight of a cat (or at least to the sight of a mobile toy that looks like a cat).

Reactions to smell were a bit more complicated. Interestingly, dogs did not spend more time investigating and sniffing the cat toy when it was baited with the smell of cat urine than they did when investigating the pee-free kitty. (Makes one wonder if the dogs were thinking……”Huh. Why did this kitty wet himself?”). Rather, the dogs spent more time sniffing the visual control (pillow case) when it was laced with cat pee than when it was pee-free. The authors suggest that there may have been a “surprise” effect occurring. Because dogs do not normally expect to smell cat pee on a pillow case (well, not in most homes, anyway), they may have spent more time investigating something that they found to be incongruent with their past experiences. There is evidence for this type of response in other circumstances with dogs in previous studies.

Last, dogs with a history of killing or injuring cats or other small animals spent significantly more time orienting to the sound of a cat meowing or growling that did dogs without such a history. These dogs did not show enhanced interest in the sight or smell of a cat, however. Although not statistically significant, dogs with a history of predation tended to orient more strongly to the control sounds also, suggesting that dogs who are not safe with cats may be hypersensitive to auditory stimuli in general.

Take Away for Dog Folks

There are several interesting things that we can learn from this study. The first is that dogs attend to cat vocalizations and may be more sensitive to cat sounds than to the sight or smell of a cat. The results with dogs who had a history of predation (either towards cats or other small animals) support the inclusion of various types of cat vocalizations when developing shelter tests that assess a dog’s reactivity to cats. While such tests require refinement and validation, it appears that including vocalizations may be helpful for differentiating between dogs who are safe with cats and dogs who may not be.

And last, dogs are interested in cat pee, especially when it shows up places where one least expects it.

This study also brings another question to mind of course – Do we need a study that distinguishes between cats who are cynophiles (dog lovers) and those who are misocynists (dog haters)?

My last Science Dog blog. “When Sit Doesn’t Mean S*it” reviewed a series of studies showing that training shelter dogs to sit on command is not as predictive of future adoption as was once assumed. Those results should not be interpreted as an argument against the benefits of training programs, but rather as evidence that there may be other factors involving shelter dogs, potential adopters and the shelter environment that may be more important to consider when looking at adoption rates and how to increase them.

Following the “sit” studies, Alexandra Protopopova and her research team set out to discover what, if anything, about dog-human visits might consistently predict adoption outcomes for dogs. They asked the question: “If sit doesn’t matter, what does?”.

What Matters: The researchers first studied 250 out-of-kennel visits between adoptable dogs and potential adopters at a municipal shelter in Florida (1). After selecting a dog to meet, shelter visitors interacted with dogs in either a small outdoor area, a larger, grassy outdoor area or a small indoor room. Multiple factors were examined during the interactions, including the dog’s appearance/breed/age, the dog’s behavior, and the visiting environment. Results: Overall, three factors stood out as significant predictors of an individual dog’s likelihood of adoption following these visits. These were:

Willingness to play: A negative relationship was found between not playing and adoption. Those dogs who ignored play initiation by visitors were less likely to be adopted than those who did not ignore the adopter’s invitation to play. The converse of this is that dogs who wanted to play with the potential adopters were more likely to be adopted after the interaction.

Lying close: Dogs who voluntarily laid down close to the human visitor were much more likely to be adopted than those who did not. (14 times as likely, in fact!)

Visiting space: Visits that took place in the small, outdoor area were more likely to lead to successful adoptions than were those that occurred in the large, enclosed grass area or in the indoor room.

LYING AT FEET AND ENGAGING IN PLAY ARE SIGNIFICANT PREDICTORS OF ADOPTION

What to do with this information? Here is where things get really cool. The researchers used the results from this study to design a simple program that could be used by shelters to improve adoption rates (2). And then, they tested the program to see if it actually worked. Science at its best.

Here is what they did:

Structured Interactions: The study included two experiments. In the first experiment, the researchers developed a play/toy preference assessment test and then used it to test the play preferences of 20 dogs. The dogs were retested several times over a period of three weeks to validate the accuracy of the tool. The second experiment used a modified version of the play preferences assessment to identify the toy preferences of a larger group of dogs at the shelter. Following their play preference testing, the dogs were assigned to two groups: (1) A structured interaction group in which potential adopters interacted with the dog with his/her preferred toy and then engaged in petting while an experimenter encouraged (lured) the dog to lie quietly at the visitors feet or (2) A control group in which the dog’s play preferences were not revealed and whose interactions with the potential adopter were unstructured. (Details of the play preference test and the structure interactions format are included in the paper). Data were collected on a total of 160 dog-adopter interactions.

Results: In the first experiment, play preference as measured by toy selection (tennis ball, nylon squeaky toy, cotton plush toy or flannel rope toy) was validated. This means that dogs who showed a preferred toy during the initial, short assessment continued to show the same preference when retested multiple times. However, it is significant to note that about one-third of the dogs (35 %) were not interested in playing with toys at all. (This is a point that the experimenters return to and address later). The import of this test lies more in the observation that simply asking dogs what type of toy that they preferred was helpful during future interactions, as found in the results of the second experiment. When the Structured Interaction group was compared with the Control group, striking differences emerged:

Dogs in the structured interactions group (offered their preferred toy, encouraged to lie down at the visitor’s feet) spent less time ignoring the visitor’s invitations to play and more time in close proximity to the visitor.

Dogs in the structured interactions group were also significantly more likely (2.5 times more likely, in fact!) to be adopted than were the control dogs.

The duration of the interactions did not differ between the two groups, suggesting that using structured interactions did not take additional staff or volunteer time than traditional visits. In addition, results of a post-interaction questionnaire revealed that the visitors did not find the format of the structured interaction to be intrusive or to interfere with their ability to visit with the dog.

Take Away for Dog Folks

There are numerous ways in which this new information may be used to help shelter dogs. The initial set of studies showed that contrary to popular belief, teaching a dog to sit does not increase his or her chance for adoption (though it very well may have other benefits). Additionally, while multiple studies have shown that a dog’s appearance is one of the strongest factors that people use when initially selecting a dog (even though people tend to deny this when asked), appearance was not found to be important during subsequent out-of-kennel visits. Rather, during the actual visit with the dog, potential adopters react more to the dog’s play behavior and tendency to stay in close proximity (lying at feet) when making their adoption decision.

Let’s first look at play behavior: The use of the play preference test in this study is in-line with our increasing understanding of the welfare and emotional health benefits seen when we allow dogs to demonstrate their preferences and even better, to have a choice. This has become a bit of a buzz-word among trainers, but hyperbole and anecdotes aside, there is really nothing not to love about a shelter dog being allowed to choose his or her favorite toy and then carrying that toy into meet-and-greet areas for play with a new visitor.

Of course, nothing will be 100 percent effective or helpful. One of the caveats of the toy preference work was the finding that not all of the dogs in the shelter were interested in playing with toys. (I am sure this is not news to shelter staff). Of the dogs tested in the 2016 study, only about 2/3 could be easily enticed to play with a toy, regardless of the toy type. This finding is consistent with previous shelter dog studies that reported that only a minority of dogs played with toys and that object-play is often of very short duration. This may occur because of the stress of the shelter environment, an individual dog’s previous history (i.e. never having had toys or opportunities to learn to play) or a combination of factors.

For those of us who live with toy (and play) maniacs, this might be surprising to learn.

LIKE ALL OF MY DOGS, CHIPPY LOVES HIS TOYS

Still, it is very helpful information. Knowing that dogs who willingly play with visitors are more often adopted and that a substantial number of shelter dogs may be reluctant to play with toys can lead shelters to develop their own innovative programs to encourage play behaviors in dogs. This may include different types of toys such as food puzzles or encouraging more “people-oriented” types of play (more about this in the next blog piece).

Second, lying in proximity: In the structured interactions group, the researchers placed the dog on lead and then used a food lure to encourage the dog to stay close and/or to lie down near the visitor. While one could argue that this behavior was not voluntary and might not reflect a truly calm dog, helping a dog to focus on relaxing and to enjoy petting would allow the visitor to experience the dog while he or she is calm and quiet in a setting that is often not conducive to calm behavior in shelter dogs. In addition, this type of relaxation training is common in many dog training programs (including my own) and can be used as a way to classically condition dogs to remain calm and enjoy handling and petting. For shelters with training programs, this information suggests that training dogs to “lie at feet in a natural environment” might be an especially important exercise to emphasize.

Last, what I personally love best about this research is that it shows science working in the very best way that it can work – first to discover new knowledge, second to create a new approach or program from that knowledge, and third to test (and in this case confirm) the validity of the new program. In my view, a win-win for everyone involved – dogs, adopters and shelter professionals.

This one has been around for a while and is almost universally accepted by shelter staff, rescue folks and dog trainers alike (including me). This is the belief that I am talking about:

“Shelter dogs who have been trained to sit on command are viewed more positively by potential adopters and are more likely to be adopted into homes.”

Makes perfect sense, of course. The “sit” command is usually one of the first things that owners teach to their new dog and is used by many trainers as the alternate behavior to reinforce not jumping up. As such, “sit” appears to have become the universal barometer for good dog behavior.

It has also become an informal litmus test for measuring shelter dog adoptability. The assumption that responding to a sit command enhances a dog’s prospects for adoption has become so commonplace that it has led to the development of shelter programs that train adoptable dogs to sit (among other commands). The goals of these programs are to increase adoption rates for the dogs who are so trained.

While there is absolutely nothing not to like about shelter programs that increase dogs’ interactions with people and introduce (positive) training, the assumption that they rest upon, that obedience training increases adoptability, has not been clearly demonstrated. Intuitively, I think most dog professionals (including myself) have believed that it does.

However, what does the science say?

Recently Alexandra Protopopova of Texas Tech University (and formerly of the University of Florida) and Clive Wynne of the University of Arizona teamed up to study the relationship between dogs’ morphology (appearance), their in-kennel behavior, and their length of stay in the shelter prior to adoption. Here is what they found:

It’s more about misbehaving: A group of 289 dogs living at a county animal shelter in Florida were videotaped for one minute daily throughout their stay (1). The one-minute time frame was selected because prior research has shown that potential adopters view a dog for only 20 to 70 seconds before moving on to the next dog. Videotaping took place as one or two visitors, behaving either passively (not interacting with the dog) or actively (interacting with the dog) visited the front of the kennel. Behaviors were classified using a validated ethogram composed of 41 standardized actions. The number of days that the dog remained at the shelter prior to adoption was used as a measure of adoptability. Results: Independently of appearance, several behaviors were significantly correlated with longer shelter stays (decreased adoptability). These included leaning passively on the kennel wall without interacting with the observer (+ 30 days), facing away from the observer (+ 15 days), and frequent movement of shifting back and forth (pacing/stereotypies) (+ 24 days). Conversely, neither sitting for greeting nor showing eye contact influenced how long a dog was at the shelter prior to adoption.

These results suggest that kennel behaviors that reflect fear or a lack of sociability are more predictive of a dog’s likelihood for adoption than are trained behaviors such as sitting to greet or offering eye contact.

Protopopova and Wynne then did what all good dog researchers do. They ran a follow-up pair of experiments to find out how best to reduce the behaviors in kenneled dogs that were shown to contribute to increased shelter stays (2).

Experiment 1: The first experiment was a pilot study to determine the effectiveness of response-dependent and response-independent treat delivery as methods to reduce the undesirable kennel behaviors identified previously. Twenty-four shelter dogs were randomly assigned to one of three experimental groups, (1) Response-independent group; the appearance of a person was paired with a treat, regardless of the dog’s behavior; (2) Response-dependent group; the experimenter Differentially Reinforced “Other” [DRO] behaviors that were incompatible with the unwanted behaviors; (3) Control; no treat delivery. Exp. 1 Results: Interestingly, they found that both treat delivery methods reduced undesirable behaviors in the kenneled dogs, with no statistical difference found between the two methods. (The control dogs continued to show undesirable behaviors).

Experiment 2: Their second experiment tested the effectiveness of the response-independent method on the entire kennel of shelter dogs. Different sections of the kennel area were used as the treatment group (visitor to kennel predicts treat) and control group (visitor does not predict treat). Between 56 and 70 dogs were enrolled each day of the 14-day experiment period. Exp. 2 Results: More than 40 percent of the shelter population regularly engaged in undesirable kennel behaviors at the start of the study. Within a few days, simply pairing the appearance of a visitor with treat delivery led to…..wait for it……a 68 % reduction in undesirable behaviors in the group of dogs as a whole.

Trainers and shelter staff everywhere should be excited about these results. While DRO is a technique that many trainers regularly use (a common example is teaching a dog to offer “sit” for greeting as an alternate behavior to jumping up), its use in a shelter environment is labor-intensive and not always feasible. However, simply pairing the appearance of a staff person with treat delivery, without requiring the treat to be contingent on the dog’s behavior is a rapid and simple technique that can be easily incorporated into daily shelter routines.

Does Sit Matter? Recently, a graduate student at Emporia State University in Kansas tested potential adopters’ inclination to adopt a dog based upon whether or not the dog sat on command (3). Her study asked a group of 79 college students to interact with a dog who they believed to be available for adoption at a local shelter. Participants were randomly assigned to a dog and then either visited with the dog as he/she sat in response to a handler’s command or interacted with the dog naturally, with no commands given to the dog. Participants then completed a questionnaire regarding their interest in adopting the dog. Results: A person’s willingness to adopt the dog that they visited with was not influenced by whether or not the dog sat on command. Similar to Protopopova’s study, sitting on command was not related to potential adoption success.

Bottom line, while responding to a sit command is a great behavior to have in our dogs, sit may not mean (much) in terms of helping shelter dogs who are looking for their forever homes.

SITS ARE GREAT, BUT EVIDENCE SUGGESTS THEY DO NOT ENHANCE ADOPTION RATES

Take Away for Dog Folks

Sad as it may seem, when it comes to a dog’s behavior, potential adopters appear to be more concerned with avoiding dogs who demonstrate behaviors that they don’t like rather than seeking dogs who show behaviors that they do like (such as responding to sit). The good news in this story is that the behaviors that people generally avoid (and which may signal a lack of sociability on the dog’s part), were demonstrated to be reduced in a substantial number of dogs without the need for a detailed and labor-intensive training program. This is classical conditioning at its best folks. Pair the approach of a visitor with yummy treats (visitor predicts treat) and over time, the appearance of a person flips the dog’s emotional response from apathy/distraction/fear to happiness, joy and interaction. The fact that the researchers improved in-kennel behaviors that were related to poor adoption rates in almost 70 percent of dogs using a simple, non-contingent procedure of food delivery is an enormously important bit of evidence. And it is evidence that can and should be used to encourage shelters everywhere to invest in treat pouches, arm their workers with a pouchful of yummy goodness and get going.

Don’t get me wrong. I personally think that training shelter dogs is a great thing. Shelter programs that teach dogs to sit, down, and walk nicely on lead are to be commended for their work and certainly should continue. However, the current science suggests that this type of training may not be as essential as we once believed and that it may not influence adoption rates. Paying more attention to reducing unwanted kennel behaviors is not only simpler, but it may be more effective as an approach to reducing shelter stays and helping dogs to be adopted into forever homes.